The Mitogenome of the Haecon-5 Strain of Haemonchus contortus and a Comparative Analysis of Its Nucleotide Variation with Other Laboratory Strains
Abstract
:1. Introduction
2. Results
2.1. The Haecon-5 Mitogenome, and Variation within an Individual and a Population
2.2. Marked Mitogenomic Variability between Haecon-5 and Other Strains
3. Discussion
4. Materials and Methods
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Emery, D.L.; Hunt, P.W.; Le Jambre, L.F. Haemonchus contortus: The then and now, and where to from here? Int. J. Parasitol. 2016, 46, 755–769. [Google Scholar] [CrossRef] [PubMed]
- Carson, A.; Reichel, R.; Bell, S.; Collins, R.; Smith, J.; Bartley, D. Haemonchus contortus: An overview. Vet. Rec. 2023, 192, 26–28. [Google Scholar] [CrossRef] [PubMed]
- Gasser, R.B.; von Samson-Himmelstjerna, G. Haemonchus contortus and Haemonchosis—Past, Present and Future Trends; Academic Press: New York, NY, USA, 2016. [Google Scholar]
- Laing, R.; Kikuchi, T.; Martinelli, A.; Tsai, I.J.; Beech, R.N.; Redman, E.; Holroyd, N.; Bartley, D.J.; Beasley, H.; Britton, C.; et al. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol. 2013, 14, R88. [Google Scholar] [CrossRef] [PubMed]
- Schwarz, E.M.; Korhonen, P.K.; Campbell, B.E.; Young, N.D.; Jex, A.R.; Jabbar, A.; Hall, R.S.; Mondal, A.; Howe, A.C.; Pell, J.; et al. The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome Biol. 2013, 14, R89. [Google Scholar] [CrossRef] [PubMed]
- Doyle, S.R.; Tracey, A.; Laing, R.; Holroyd, N.; Bartley, D.; Bazant, W.; Beasley, H.; Beech, R.; Britton, C.; Brooks, K.; et al. Genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm. Commun. Biol. 2020, 3, 656. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Ma, G.; Ang, C.S.; Korhonen, P.K.; Koehler, A.V.; Young, N.D.; Nie, S.; Williamson, N.A.; Gasser, R.B. High throughput LC-MS/MS-based proteomic analysis of excretory-secretory products from short-term in vitro culture of Haemonchus contortus. J. Proteom. 2019, 204, 103375. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Ma, G.; Nie, S.; Williamson, N.A.; Reid, G.E.; Gasser, R.B. Lipid composition and abundance in the reproductive and alimentary tracts of female Haemonchus contortus. Parasit. Vectors 2020, 13, 338. [Google Scholar] [CrossRef] [PubMed]
- Sallé, G.; Doyle, S.R.; Cortet, J.; Cabaret, J.; Berriman, M.; Holroyd, N.; Cotton, J.A. The global diversity of Haemonchus contortus is shaped by human intervention and climate. Nat. Commun. 2019, 10, 4811. [Google Scholar] [CrossRef]
- Jex, A.R.; Hu, M.; Littlewood, D.T.; Waeschenbach, A.; Gasser, R.B. Using 454 technology for long-PCR based sequencing of the complete mitochondrial genome from single Haemonchus contortus (Nematoda). BMC Genom. 2008, 9, 11. [Google Scholar] [CrossRef]
- Palevich, N.; Maclean, P.; Baten, A.; Scott, R.; Leathwick, D.M. The complete mitochondrial genome of the New Zealand parasitic roundworm Haemonchus contortus (Trichostrongyloidea: Haemonchidae) field strain NZ_Hco_NP. Mitochondrial DNA B Resour. 2019, 4, 2208–2210. [Google Scholar] [CrossRef] [PubMed]
- Blouin, M.S.; Yowell, C.A.; Courtney, C.H.; Dame, J.B. Host movement and the genetic structure of populations of parasitic nematodes. Genetics 1995, 141, 1007–1014. [Google Scholar] [CrossRef] [PubMed]
- Hu, M.; Chilton, N.B.; Gasser, R.B. The mitochondrial genomics of parasitic nematodes of socio-economic importance: Recent progress, and implications for population genetics and systematics. Adv. Parasitol. 2004, 56, 133–212. [Google Scholar] [CrossRef] [PubMed]
- Hu, M.; Gasser, R.B. Mitochondrial genomes of parasitic nematodes-progress and perspectives. Trends Parasitol. 2006, 22, 78–84. [Google Scholar] [CrossRef] [PubMed]
- Brasil, B.S.; Nunes, R.L.; Bastianetto, E.; Drummond, M.G.; Carvalho, D.C.; Leite, R.C.; Molento, M.B.; Oliveira, D.A. Genetic diversity patterns of Haemonchus placei and Haemonchus contortus populations isolated from domestic ruminants in Brazil. Int. J. Parasitol. 2012, 42, 469–479. [Google Scholar] [CrossRef] [PubMed]
- Yin, F.; Gasser, R.B.; Li, F.; Bao, M.; Huang, W.; Zou, F.; Zhao, G.; Wang, C.; Yang, X.; Zhou, Y.; et al. Genetic variability within and among Haemonchus contortus isolates from goats and sheep in China. Parasit. Vectors 2013, 6, 279. [Google Scholar] [CrossRef] [PubMed]
- Pitaksakulrat, O.; Chaiyasaeng, M.; Artchayasawat, A.; Eamudomkarn, C.; Boonmars, T.; Kopolrat, K.Y.; Prasopdee, S.; Petney, T.N.; Blair, D.; Sithithaworn, P. Genetic diversity and population structure of Haemonchus contortus in goats from Thailand. Infect. Genet. Evol. 2021, 95, 105021. [Google Scholar] [CrossRef] [PubMed]
- Ma, G.; Gasser, R.B.; Wang, T.; Korhonen, P.K.; Young, N.D. Toward integrative ‘omics of the barber’s pole worm and related parasitic nematodes. Infect. Genet. Evol. 2020, 85, 104500. [Google Scholar] [CrossRef] [PubMed]
- Ma, G.; Wang, T.; Korhonen, P.K.; Ang, C.S.; Williamson, N.A.; Young, N.D.; Stroehlein, A.J.; Hall, R.S.; Koehler, A.V.; Hofmann, A.; et al. Molecular alterations during larval development of Haemonchus contortus in vitro are under tight post-transcriptional control. Int. J. Parasitol. 2018, 48, 763–772. [Google Scholar] [CrossRef] [PubMed]
- Ma, G.; Wang, T.; Korhonen, P.K.; Stroehlein, A.J.; Young, N.D.; Gasser, R.B. Dauer signalling pathway model for Haemonchus contortus. Parasit. Vectors 2019, 12, 187. [Google Scholar] [CrossRef] [PubMed]
- Redman, E.; Grillo, V.; Saunders, G.; Packard, E.; Jackson, F.; Berriman, M.; Gilleard, J.S. Genetics of mating and sex determination in the parasitic nematode Haemonchus contortus. Genetics 2008, 180, 1877–1887. [Google Scholar] [CrossRef] [PubMed]
- Redman, E.; Sargison, N.; Whitelaw, F.; Jackson, F.; Morrison, A.; Bartley, D.J.; Gilleard, J.S. Introgression of ivermectin resistance genes into a susceptible Haemonchus contortus strain by multiple backcrossing. PLoS Pathog. 2012, 8, e1002534. [Google Scholar] [CrossRef] [PubMed]
- Rezansoff, A.M.; Laing, R.; Martinelli, A.; Stasiuk, S.; Redman, E.; Bartley, D.; Holroyd, N.; Devaney, E.; Sargison, N.D.; Doyle, S.; et al. The confounding effects of high genetic diversity on the determination and interpretation of differential gene expression analysis in the parasitic nematode Haemonchus contortus. Int. J. Parasitol. 2019, 49, 847–858. [Google Scholar] [CrossRef] [PubMed]
- Sargison, N.D.; Redman, E.; Morrison, A.A.; Bartley, D.J.; Jackson, F.; Hoberg, E.; Gilleard, J.S. Mating barriers between genetically divergent strains of the parasitic nematode Haemonchus contortus suggest incipient speciation. Int. J. Parasitol. 2019, 49, 531–540. [Google Scholar] [CrossRef] [PubMed]
- Taki, A.C.; Byrne, J.J.; Wang, T.; Sleebs, B.E.; Nguyen, N.; Hall, R.S.; Korhonen, P.K.; Chang, B.C.H.; Jackson, P.; Jabbar, A.; et al. High-throughput phenotypic assay to screen for anthelmintic activity on Haemonchus contortus. Pharmaceuticals 2021, 14, 616. [Google Scholar] [CrossRef] [PubMed]
- Taki, A.C.; Wang, T.; Nguyen, N.N.; Ang, C.S.; Leeming, M.G.; Nie, S.; Byrne, J.J.; Young, N.D.; Zheng, Y.; Ma, G.; et al. Thermal proteome profiling reveals Haemonchus orphan protein HCO_011565 as a target of the nematocidal small molecule UMW-868. Front. Pharmacol. 2022, 13, 1014804. [Google Scholar] [CrossRef] [PubMed]
- Morrison, A.A.; Chaudhry, U.; Andrews, L.; Melville, L.; Doyle, S.R.; Sargison, N.D.; Bartley, D.J. Phenotypic and genotypic analysis of benzimidazole resistance in reciprocal genetic crosses of Haemonchus contortus. Int. J. Parasitol. Drugs Drug Resist. 2022, 18, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Ma, G.; Wang, T.; Hofmann, A.; Song, J.; Gasser, R.B.; Young, N.D. Ubiquitination pathway model for the barber’s pole worm-Haemonchus contortus. Int. J. Parasitol. 2022, 52, 581–590. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Young, N.D.; Song, J.; Chang, B.C.H.; Gasser, R.B. An informatic workflow for the enhanced annotation of excretory/secretory proteins of Haemonchus contortus. Comput. Struct. Biotechnol. J. 2023, 21, 2696–2704. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Young, N.D.; Song, J.; Gasser, R.B. Genome-wide analysis of Haemonchus contortus proteases and protease inhibitors using advanced informatics provides insights into parasite biology and host-parasite interactions. Int. J. Mol. Sci. 2023, 24, 12320. [Google Scholar] [CrossRef] [PubMed]
- Veglia, F. The anatomy and life-history of the Haemonchus contortus (Rud.). Rep. Dir. Vet. Res. 1915, 3, 347–500. [Google Scholar]
- Das, K.M.; Whitlock, J.H. Subspeciation in Haemonchus contortus (Rudolphi, 1803) Nemata, Trichostrongyloidea. Cornell. Vet. 1960, 50, 182–197. [Google Scholar] [PubMed]
- Lichtenfels, J.R.; Pilitt, P.A.; Hoberg, E.P. New morphological characters for identifying individual specimens of Haemonchus spp. (Nematoda: Trichostrongyloidea) and a key to species in ruminants of North America. J. Parasitol. 1994, 80, 107–119. [Google Scholar] [CrossRef] [PubMed]
- Rahman, W.A.; Abd Hamid, S. Morphological characterization of Haemonchus contortus in goats (Capra hircus) and sheep (Ovis aries) in Penang, Malaysia. Trop. Biomed. 2007, 24, 23–27. [Google Scholar] [PubMed]
- Hunt, P.W.; Knox, M.R.; Le Jambre, L.F.; McNally, J.; Anderson, L.J. Genetic and phenotypic differences between isolates of Haemonchus contortus in Australia. Int. J. Parasitol. 2008, 38, 885–900. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Ortiz-de-Montellano, C.; Torres-Acosta, J.F.J.; Sandoval-Castro, C.A.; Fourquaux, I.; Hoste, H. Scanning electron microscopy of different vulval structures in a Mexican Haemonchus contortus isolate. Vet. Parasitol. Reg. Stud. Rep. 2021, 26, 100640. [Google Scholar] [CrossRef] [PubMed]
- Vongnady, K.; Rucksaken, R.; Mangkit, B. Cuticular ridge patterns applied for identifying adult female worms of Haemonchus species with various vulvar morphological types in infected native goats in Laos. Trop. Biomed. 2021, 38, 294–310. [Google Scholar] [CrossRef] [PubMed]
- Tsang, W.Y.; Lemire, B.D. Mitochondrial genome content is regulated during nematode development. Biochem. Biophys. Res. Commun. 2002, 291, 8–16. [Google Scholar] [CrossRef] [PubMed]
- Tsang, W.Y.; Lemire, B.D. The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim. Biophys. Acta 2003, 1638, 91–105. [Google Scholar] [CrossRef] [PubMed]
- Estes, S.; Dietz, Z.P.; Katju, V.; Bergthorsson, U. Evolutionary codependency: Insights into the mitonuclear interaction landscape from experimental and wild Caenorhabditis nematodes. Curr. Opin. Genet. Dev. 2023, 81, 102081. [Google Scholar] [CrossRef] [PubMed]
- Konrad, A.; Thompson, O.; Waterston, R.H.; Moerman, D.G.; Keightley, P.D.; Bergthorsson, U.; Katju, V. Mitochondrial mutation rate, spectrum and heteroplasmy in Caenorhabditis elegans spontaneous mutation accumulation lines of differing population size. Mol. Biol. Evol. 2017, 34, 1319–1334. [Google Scholar] [CrossRef]
- Kinkar, L.; Gasser, R.B.; Webster, B.L.; Rollinson, D.; Littlewood, D.T.J.; Chang, B.C.H.; Stroehlein, A.J.; Korhonen, P.K.; Young, N.D. Nanopore sequencing resolves elusive long tandem-repeat regions in mitochondrial genomes. Int. J. Mol. Sci. 2021, 22, 1811. [Google Scholar] [CrossRef] [PubMed]
- Koren, S.; Walenz, B.P.; Berlin, K.; Miller, J.R.; Bergman, N.H.; Phillippy, A.M. Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017, 27, 722–736. [Google Scholar] [CrossRef] [PubMed]
- Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28, 1647–1649. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef]
- Jeffares, D.C.; Tomiczek, B.; Sojo, V.; dos Reis, M. A beginners guide to estimating the non-synonymous to synonymous rate ratio of all protein-coding genes in a genome. Methods Mol. Biol. 2015, 1201, 65–90. [Google Scholar] [CrossRef] [PubMed]
- Brown, S.D.; Collins, R.A.; Boyer, S.; Lefort, M.C.; Malumbres-Olarte, J.; Vink, C.J.; Cruickshank, R.H. Spider: An R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Mol. Ecol. Resour. 2012, 12, 562–565. [Google Scholar] [CrossRef] [PubMed]
- Lawrence, M.; Huber, W.; Pagès, H.; Aboyoun, P.; Carlson, M.; Gentleman, R.; Morgan, M.T.; Carey, V.J. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 2013, 9, e1003118. [Google Scholar] [CrossRef] [PubMed]
- Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [PubMed]
Features | Haecon-5 [This Study] | MHco3(ISE).N1 Ref. [6] | McMaster Ref. [10] | NZ_Hco_NP Ref. [11] |
---|---|---|---|---|
Mitochondrial genome size (bp) | 14,107 | 14,018 | 14,055 | 14,001 |
Number of genes | 36 | 36 | 36 | 36 |
Number of protein-coding genes | 12 | 12 | 12 | 12 |
Number of tRNA genes | 22 | 22 | 22 | 22 |
Number of rRNA genes | 2 | 2 | 2 | 2 |
A (%) | 33.0 | 33.2 | 33.4 | 32.9 |
C (%) | 6.4 | 6.5 | 6.5 | 6.3 |
G (%) | 15.6 | 15.5 | 15.4 | 14.8 |
T (%) | 44.9 | 44.9 | 44.7 | 44.5 |
GC (%) | 22.0 | 21.9 | 21.9 | 21.1 |
AT (%) | 78.0 | 78.1 | 78.0 | 78.9 |
Predominant start codon | ATA | ATA | ATA | ATA |
Predominant stop codon | TAA | TAA | TAA | TAA |
Gene Name or Region | Description | Start | End | Length (bp) | Number of SNPs | Number of Indels | Number of MNPs | Total Number of Nucleotide Alterations |
---|---|---|---|---|---|---|---|---|
cox1 | CDS | 1 | 1582 | 1582 | 38[0] | 0 | 0 | 38[0] |
cox2 | CDS | 1861 | 2553 | 693 | 18[0] | 0 | 1[0] | 19[0] |
nad3 | CDS | 3555 | 3881 | 327 | 6[0] | 0 | 0 | 6[0] |
nad5 | CDS | 3892 | 5473 | 1582 | 31[4] | 0 | 0 | 31[4] |
nad6 | CDS | 6362 | 6790 | 429 | 12[5] | 0 | 1[1] | 13[6] |
nad4L | CDS | 6797 | 7028 | 232 | 2[0] | 0 | 0 | 2[0] |
nad1 | CDS | 8044 | 8916 | 873 | 29[4] | 0 | 0 | 29[4] |
atp6 | CDS | 8918 | 9517 | 600 | 12[2] | 0 | 0 | 12[2] |
nad2 | CDS | 9704 | 10,549 | 846 | 14[3] | 0 | 1[1] | 15[4] |
cytb | CDS | 10,816 | 11,928 | 1113 | 32[4] | 0 | 0 | 32[4] |
cox3 | CDS | 11,986 | 12,754 | 769 | 16[0] | 0 | 0 | 16[0] |
nad4 | CDS | 12,807 | 14,036 | 1230 | 28[3] | 0 | 0 | 28[3] |
trnC | tRNA | 1583 | 1636 | 54 | 1 | 0 | 0 | 1 |
trnM | tRNA | 1648 | 1704 | 57 | 0 | 0 | 0 | 0 |
trnD | tRNA | 1728 | 1784 | 57 | 0 | 0 | 0 | 0 |
trnG | tRNA | 1806 | 1860 | 55 | 1 | 0 | 0 | 1 |
trnH | tRNA | 2554 | 2606 | 53 | 1 | 0 | 0 | 1 |
trnA | tRNA | 5474 | 5530 | 57 | 0 | 0 | 0 | 0 |
trnP | tRNA | 6195 | 6250 | 56 | 0 | 1 | 0 | 1 |
trnV | tRNA | 6289 | 6343 | 55 | 1 | 0 | 0 | 1 |
trnW | tRNA | 7029 | 7085 | 57 | 0 | 0 | 0 | 0 |
trnE | tRNA | 7098 | 7152 | 55 | 0 | 0 | 0 | 0 |
trnS | tRNA | 7853 | 7907 | 55 | 0 | 0 | 0 | 0 |
trnN | tRNA | 7930 | 7985 | 56 | 1 | 0 | 0 | 1 |
trnY | tRNA | 7990 | 8043 | 54 | 2 | 0 | 0 | 2 |
trnK | tRNA | 9532 | 9588 | 57 | 0 | 1 | 0 | 1 |
trnL | tRNA | 9597 | 9651 | 55 | 0 | 0 | 0 | 0 |
trnS | tRNA | 9652 | 9703 | 52 | 1 | 0 | 0 | 1 |
trnI | tRNA | 10,561 | 10,619 | 59 | 0 | 0 | 0 | 0 |
trnR | tRNA | 10,620 | 10,675 | 56 | 0 | 0 | 0 | 0 |
trnE | tRNA | 10,676 | 10,730 | 55 | 1 | 0 | 0 | 1 |
trnF | tRNA | 10,762 | 10,815 | 54 | 0 | 0 | 0 | 0 |
trnL | tRNA | 11,929 | 11,985 | 57 | 0 | 2 | 0 | 2 |
trnT | tRNA | 12,753 | 12,808 | 56 | 0 | 0 | 0 | 0 |
rrnL | rRNA | 2607 | 3557 | 951 | 6 | 0 | 0 | 6 |
rrnS | rRNA | 7151 | 7852 | 702 | 3 | 1 | 0 | 4 |
AT-rich region | non-coding | 5531 | 6194 | 663 | 20 | 6 | 0 | 26 |
Comparisons | Number of | Protein-Coding Genes | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
SNPs; Indels; MNPs | Nucleotide Alterations (Total) | cox1 | cox2 | nad3 | nad5 | nad6 | nad4L | nad1 | atp6 | nad2 | cytb | cox3 | nad4 | |
Haecon-5 vs. MHco3(ISE).N1 | 345[31]; 16[0]; 7[4] | 368[35] | 41[0] | 22[0] | 7[0] | 37[6] | 18[6] | 3[0] | 36[5] | 16[5] | 22[7] | 32[3] | 21[1] | 23[2] |
Haecon-5 vs. McMaster | 344[31]; 20 (0); 14[5] | 378[36] | 42[0) | 25[2] | 7[0] | 38[7] | 23[5] | 4[1] | 28[5] | 19[2] | 15[4] | 31[5] | 22[2] | 29[3] |
Haecon-5 vs. NZ_Hco_NP | 435[25]; 16[0]; 9[5] | 460[30] | 60[0] | 29[1] | 9[1] | 44[8] | 15[3] | 4[0] | 27[6] | 19[3] | 24[3] | 38[2] | 36[1] | 50[2] |
Among all strains | 695[57]; 36[0]; 14[6] | 745[63] | 88[0] | 43[3] | 12[1] | 71[12] | 34[9] | 8[1] | 55[10] | 37[6] | 38[9] | 59[5] | 50[4] | 59[3] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zheng, Y.; Young, N.D.; Song, J.; Gasser, R.B. The Mitogenome of the Haecon-5 Strain of Haemonchus contortus and a Comparative Analysis of Its Nucleotide Variation with Other Laboratory Strains. Int. J. Mol. Sci. 2024, 25, 8765. https://doi.org/10.3390/ijms25168765
Zheng Y, Young ND, Song J, Gasser RB. The Mitogenome of the Haecon-5 Strain of Haemonchus contortus and a Comparative Analysis of Its Nucleotide Variation with Other Laboratory Strains. International Journal of Molecular Sciences. 2024; 25(16):8765. https://doi.org/10.3390/ijms25168765
Chicago/Turabian StyleZheng, Yuanting, Neil D. Young, Jiangning Song, and Robin B. Gasser. 2024. "The Mitogenome of the Haecon-5 Strain of Haemonchus contortus and a Comparative Analysis of Its Nucleotide Variation with Other Laboratory Strains" International Journal of Molecular Sciences 25, no. 16: 8765. https://doi.org/10.3390/ijms25168765